BRIEF RESEARCH REPORT published: 30 April 2021 doi: 10.3389/fpubh.2021.670669

Occupational Characteristics and Management Measures of Sporadic COVID-19 Outbreaks From June 2020 to January 2021 in : The Importance of Tracking Down “Patient Zero”

Maohui Feng 1†, Qiong Ling 2†, Jun Xiong 3, Anne Manyande 4, Weiguo Xu 5 and Boqi Xiang 6*

1 Department of Gastrointestinal Surgery, Peritoneal Cancer Clinical Medical Research Center, Hubei Key Laboratory of Tumor Biological Behaviors, Hubei Cancer Clinical Study Center, Zhongnan Hospital of Wuhan University, Wuhan, China, 2 Department of Anesthesiology, The Second Affiliated Hospital of Guangzhou University of Chinese Medicine, Guangzhou, China, 3 Hepatobiliary Surgery Center, Union Hospital of Tongji Medical College, Huazhong University of Science and Technology, Wuhan, China, 4 School of Human and Social Sciences, University of West London, London, United Kingdom, Edited by: 5 Department of Orthopedics, Tongji Hospital of Tongji Medical College, Huazhong University of Science and Technology, Henri Heussen, Wuhan, China, 6 School of Public Health, University of Rutgers, New Brunswick, NJ, United States Cosanta BV, Netherlands Reviewed by: There are occupational disparities in the risk of contracting COVID-19. Occupational Andrea Spinazzè, University of Insubria, Italy characteristics and work addresses play key roles in tracking down “patient zero.” The Antonio Caputi, present descriptive analysis for occupational characteristics and management measures University of Bari Aldo Moro, Italy of sporadic COVID-19 outbreaks from June to December offers important *Correspondence: new information to the international community at this stage of the pandemic. These Boqi Xiang [email protected] data suggest that Chinese measures including tracking down “patient zero,” launching mass COVID-19 testing in the SARS-CoV-2-positive areas, designating a new high- or †These authors have contributed equally to this work medium-risk area, locking down the corresponding community or neighborhood in response to new COVID-19 cases, and basing individual methods of protection on Specialty section: science are effective in reducing the transmission of the highly contagious SARS-CoV-2 This article was submitted to Occupational Health and Safety, across China. a section of the journal Keywords: COVID-19 disease, severe acute respiratory syndrome coronavirus 2, patient zero, sporadic cases, Frontiers in Public Health occupational characteristics, protective measures, person-to-person transmission Received: 02 March 2021 Accepted: 29 March 2021 Published: 30 April 2021 INTRODUCTION Citation: Feng M, Ling Q, Xiong J, The transmission of the novel severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) Manyande A, Xu W and Xiang B includes the fomite route through contacts, droplet-borne route transmitted by medium or (2021) Occupational Characteristics large droplets, and airborne route through aerosols that can remain suspended over a longer and Management Measures of time (1–6). COVID-19 outbreaks not only highlighted the vulnerability of many patients and Sporadic COVID-19 Outbreaks From residents, but also the limited clinical support that led to international headlines. The World June 2020 to January 2021 in China: The Importance of Tracking Down Health Organization (WHO) declared a “public health emergency of international concern” and “Patient Zero.” “pandemic of COVID-19” on January 30, 2020 and March 11, 2020, respectively (7–10). By January Front. Public Health 9:670669. 26, 2021, more than 100 million COVID-19 cases have been reported in more than 188 countries, doi: 10.3389/fpubh.2021.670669 resulting in over 2.14 million deaths worldwide.

Frontiers in Public Health | www.frontiersin.org 1 April 2021 | Volume 9 | Article 670669 Feng et al. Tracking Down Patient Zero

With much of the world still in the grips of the pandemic track this epidemic, collect its epidemiological characteristics COVID-19, importation of the SARS-CoV-2 virus poses a great from announcements by the local Health Commission, and potential threat to epidemic prevention and control in China. present a descriptive analysis for occupational characteristics Though China took a number of strict measures to prevent and management measures of sporadic outbreaks of COVID-19 importing the virus via inbound travelers and imported goods (from June to December 2020). over the past few months, local sporadic outbreaks of COVID- Publicly available information was compiled from 19 were reported from June 2020 to January 2021. In these announcements by local authorities from the China Center new sporadic outbreak regions, detection of “No. 0 source for Disease Control and Prevention, the National Health of infection” is crucial work. It is well-known that there are Commission in Tianjin, Beijing, Qingdao, Dalian, Shenyang, occupational disparities in the risk of contracting COVID-19 Shanghai, and the WHO. We also searched reports from (11). “Patient zero” refers to the first human infected by the the media and announcements from the local Municipal virus in a new outbreak region, which may be one or more Health Commissions related to patient zero or cold-chain food confirmed/asymptomatic cases. Occupational characteristics and transmission infection control from June to January 2021. Also, work addresses of “patient zero” play key roles in tracking down we collected literature using the PubMed database and Cochrane “No. 0 source of infection” (12). We collected and analyzed Library from June 1, 2019 to January 31, 2021. Search terms data on occupational characteristics and management measures included “patient zero” and “novel coronavirus” or “COVID-19” tackling COVID-19 in China. or “2019-nCoV”.

METHODS RESULTS

At the beginning of June 1, 2020, we prospectively focus on the Occupational Distribution of “Patient Zero” COVID-19 epidemic data from the Chinese Center for Disease in Local Sporadic Outbreak Regions Control and Prevention every day. Once receiving the new Tracing “No. 0 source of infection” is crucial work in new report of a confirmed or asymptomatic case in China, we will sporadic outbreak regions. From June to December 2020, the

FIGURE 1 | Geographical and occupational distribution of local sporadic outbreak cases with COVID-19 from June to December 2020. Five cities (Dalian, Tianjin, Qingdao, Kashgar, and Shanghai) reported the “patient zero.” For the outbreak in Kashgar and Shanghai, the source of the epidemic was frozen or wet containers outside the border and their “patient zero” was container stevedore who was asymptomatic. Plaza business hall staff (1) in Urumqi (July 15), supermarket employees (1) in Shenzhen (August 14), truck driver (1) in Hong Kong (July 26), Food delivery staff (1) and food production workers (8) in Beijing (June 21) were diagnosed as confirmed cases.

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TABLE 1 | Data of identified “patient zero” in new sporadic outbreak regions.

City Date Patient zero Occupation Diagnosis Source of infection

Dalian July 22 2 Transportation worker Asymptomatic case Cold-food Qingdao October 11 2 Container handler Asymptomatic case Cold seafood Kashi October 24 2 Container stevedore Asymptomatic case Imported containers Shanghai November 9 2 Container handler Confirmed case Imported containers Tianjin November 9 1 Transportation worker Asymptomatic case Cold-food

FIGURE 2 | The graph’s left-right axis (dates from June to December 2020) is used as a timeline of the key events and dynamic profile of “patient zero” during the local sporadic COVID-19 outbreak. From June to December 2020, five cities in China had reported over nine “patient zero,” including two confirmed cases and seven asymptomatic cases. On October 27, NHC issued Q&A of COVID-19 prevention and control Technology Guide for cold chain food production and COVID-19 prevention and Control Disinfection Technology Guide for cold chain food. The contents include hygiene management measures at the source of cold chain goods, prevention and control requirements in the process of production and processing, prevention and control requirements in the process of sales and operation, cleaning and disinfection operations in the process of cold chain food production and processing and precautions for disinfection of equipment or surfaces of environmental objects. On November 27, the Chinese Ministry of Transport issued a comprehensive guideline to lower the risk of virus transmission via cold chain logistics. occupational distribution of patient zero in local sporadic SARS-CoV-2 was detected on imported frozen raw foods, mostly outbreak regions with COVID-19 is shown in Figure 1. Data on their packaging materials (Figure 3). During the outbreak in of identified “patient zeros” in new sporadic outbreak regions Beijing, five fish swab samples related to imported cold chain are presented in Table 1. From June to December 2020, five food (Salmon) tested positive for SARS-CoV-2 nucleic acid in cities in China had reported over nine “patient zeros,” including the Xinfadi market and the virus genome sequence obtained two confirmed cases and seven asymptomatic cases (Figure 2 from one unopened fish swab sample was highly homologous and Table 1). These “patient zeros” may be involved in a to the virus in human and environmental samples in this cold-chain environment-to-human transmission of COVID-19 epidemic. As for the outbreak in Qingdao, the live SARS-CoV- (Table 1). For the outbreak in Kashgar and Shanghai, the source 2 virus was successfully isolated from the imported frozen cod of the epidemic was frozen or wet containers outside the package surfaces. border and their “patient zero” was container stevedore who In addition, the novel coronavirus SARS-CoV-2 was found was asymptomatic. on frozen food surfaces, packaging materials and food storage In addition, plaza business hall staff (1) in Urumqi (July 15), environments in many cities, for example Dalian (July 3), Xiamen supermarket employees (1) in Shenzhen (August 14), truck driver (July 3) Shenzhen (August 12), etc. (1) in Hong Kong (July 26), and Food delivery staff (1) and food production workers (8) in Beijing (June 21) were diagnosed as Epidemiological Characteristics and confirmed cases (Figure 1). Occupational Distribution of Sporadic Nosocomial COVID-19 Infections Detection of SARS-CoV-2 on Imported Epidemiological characteristics and occupational distribution Frozen Raw Foods and Their Packaging of sporadic nosocomial COVID-19 infections is presented Materials Across China in Table 2. From June 2020 to January 2021, six hospitals Since the beginning of June 2020, at least 10 incidents of food in China had reported over 23 confirmed cases. Among contamination have been reported across the country, where them, nursing staff (3), doctors (4), cleaner (1), patients (4)

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FIGURE 3 | ARS-CoV-2 detection on imported frozen raw foods and their packaging materials across China. During the outbreak in Beijing, five fish swab samples related to imported cold chain food (Salmon) tested positive for SARS-CoV-2 nucleic acid in Xinfadi market. As for the outbreak in Qingdao, the live SARS-CoV-2 virus was successfully isolated from the imported frozen cod package surfaces. The SARS-CoV-2 was also found on frozen food surfaces, packaging materials and food storage environments in many cities, for example Dalian (July 3), Xiamen (July 3) Shenzhen (August 12), etc.

TABLE 2 | Epidemiological characteristics of sporadic nosocomial COVID-19 infections.

Date City Number of Confirmed cases Profession Route of infection hospitals

June 14 Beijing 1 1 Nurse Family member exposure with COVID-19 October 11 Qingdao 1 6 Patients and accompanying staffs Nosocomial infection October 29 Qingdao 1 1 Nurse Workplace accidental exposure to COVID-19 December 27 Dalian 1 1 Cleaner Cold-chain environment-to-human transmission January 3 Shenyang 1 12 Medical staff, patients and accompanying staffs Nosocomial infection January 20 Shanghai 2 2 Logistics support staffs Imported from overseas

accompanying staff (9), and logistics support staff (2) were the occupational distribution of sporadic nosocomial COVID- diagnosed. The route of infection mainly included workplace 19 infections. Chinese management measures including tracking accidental exposure to COVID-19, nosocomial infection between down “patient zero,” launching mass COVID-19 testing in healthcare workers and patients, family member exposure with SARS-CoV-2-positive areas, designating a new high or medium- COVID-19, cold-chain environment-to-human transmission risk area, locking down the corresponding community or and imported from overseas. neighborhood in response to new COVID-19 cases, and basing individual methods of protection on science were all found DISCUSSION to be effective in rapidly reducing transmission of the highly contagious SARS-CoV-2 across China. A main finding of the occupational characteristics of new Based on the WHO’s definition, transmission classifications sporadic outbreaks with COVID-19 from June 2020 to January of the contagious disease include no confirmed cases, sporadic 2021 in China was central to tracking down “patient zero.” cases, clusters of cases and community transmission. Sporadic Here we offered a first description of the occupational cases are defined as cities/areas with one or more cases, distribution of “patient zero,” epidemiological characteristics and imported or locally detected. Clusters of cases refer to cities/areas

Frontiers in Public Health | www.frontiersin.org 4 April 2021 | Volume 9 | Article 670669 Feng et al. Tracking Down Patient Zero experiencing cases, clustered in time, geographic location patients is important during a period of community prevalence and/or by common exposures. Community transmission are of COVID-19 (18). The data showed that extreme caution defined as cities/areas experiencing larger outbreaks of local of authorities, high-grade protection, and social distancing transmission defined through an assessment of factors including, were crucial strategies of hospital prevention and protection but not limited to: (1) Large numbers of cases not linkable to measures (20, 21). Dantes et al. (22) reported that delayed transmission chains; (2) Large numbers of cases from sentinel recognition of community transmission of covid-19 resulted lab surveillance; (3) Multiple unrelated clusters in several areas in healthcare worker infections. Jones et al. (23) showed of the country/cities/areas (13). Based on the above analyses, we that the proportion of both asymptomatic and symptomatic suggest that SARS-CoV-2 infections in six cities belong to new healthcare workers (HCWs) testing positive for SARS-CoV-2 sporadic outbreaks of COVID-19 from June 2020 to January 2021 rapidly declined to near-zero between 25th April and 24th May in China. 2020, which corresponded to the decline in patient admissions In new sporadic outbreak regions, tracing “patient zero,” also with COVID-19 during the ongoing UK “lockdown,” suggesting known as the index case, is important work. “Patient zero” refers that infection prevention and control measures may help prevent to the first human infected by the virus in a new outbreak hospitals from becoming independent ‘hubs’ of SARS-CoV- region, which may be one or more confirmed/asymptomatic 2 transmission. Our data indicated that Chinese scientific cases. Tracking down “patient zero” could provide new insights measures could effectively curb the nosocomial spread of for epidemiologists and local authorities about the nature of first the COVID-19. transmissions into a population and to understanding the novel In conclusion, the present analysis of occupational SARS-CoV-2 virus behind the ongoing global health crisis and characteristics and management measures of sporadic COVID- how to curb further transmission (14). In many hard-hit regions, 19 outbreaks from June 2020 to December 2021 in China offers it was difficult to know how the SARS-CoV-2 virus got there important information to the international community. Chinese or who contracted it first (15). But in new sporadic outbreak scientific measures including tracking down “patient zero” or regions, we recommend that identifying “patient zero” may be “No. 0 source of infection,” launching mass COVID-19 testing more useful. Our data showed that five cities in China reported and individual methods of protection based on science are crucial over nine “patient zeros” from June to December 2020. strategies to curb further spread of COVID-19 and prevent the The potential role of the environment-to-person transmission importation of the SARS-CoV-2 virus via inbound travelers and spread of COVID-19 highlights the importance of detecting “No. imported goods. 0 source of infection” and tracking down “patient zero.” Jones et al. (16) reported the shedding of SARS-CoV-2 in feces and DATA AVAILABILITY STATEMENT urine and its potential role in person-to-person transmission and the environment-based spread of COVID-19. Our data showed The original contributions presented in the study are included that imported frozen raw foods and their packaging materials in the article/supplementary material, further inquiries can be tested positive for SARS-CoV-2 nucleic acid, suggesting that the directed to the corresponding author. “No. 0 source of infection” and “patient zero” are involved in cold-chain environment-to-human transmission of COVID-19. AUTHOR CONTRIBUTIONS The outbreak of SARS-CoV-2 virus places medical staff at an increased risk of infection as they are in close contact MF, QL, and JX: data collection. WX, AM, and BX: data with patients with COVID-19 (17–19). Effective control of interpretation and writing. All authors contributed to the article SARS-CoV-2 transmission between healthcare workers and and approved the submitted version.

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